the effect of manure and the bioaccumulation of heavy metals … · sengon (paraserianthes...

Advanced Studies in Biology, Vol. 8, 2016, no. 2, 77 - 89

HIKARI Ltd, www.m-hikari.com

http://dx.doi.org/10.12988/asb.2016.6411

The Effect of Manure and the Bioaccumulation of

Heavy Metals Hg, Cu and Zn at Ex-Gold Mining

Land on the Growth of Silk Tree (Paraserinthes

falcataria (L.) Nielsen) in Bombana,

Southeast Sulawesi

Sri Ambardini a, Darwis b, La Ode Safuan b, Ahmad Zaeni c and Asrul Sani *d

a Department of Biology, Faculty of Mathematics and Natural Sciences

Universitas Halu Oleo, Kendari, Indonesia

b Department of Agrotechnology, Faculty of Agriculture


c Department of Chemistry, Faculty of Mathematics and Natural Sciences


d Department of Mathematics, Faculty of Mathematics and Natural Sciences

Universitas Halu Oleo, Kendari, Indonesia *Corresponding author

Copyright © 2016 Sri Ambardini et al. This article is distributed under the Creative Commons

Attribution License, which permits unrestricted use, distribution, and reproduction in any medium,

provided the original work is properly cited.

Abstract

One of the negative effects of gold mining activity is soil contamination by

heavy metal. The aims of this study were two folds; to assess the effect of

manures (cow, goat, chicken) (i) on the growth of silk tree (Paraserianthes

falcataria (L.) Nielsen) and (ii) on the bioaccumulation of heavy metals (Hg, Cu,

Zn) in the plant organs of the silk tree planted in the ex-gold mining land in

Bombana. This is an experimental research design with a completely randomized

78 Sri Ambardini et al.

design consisting of one control (without manure) and 4 treatments (cow, goat and

chicken manures) with 5 repplicates. The plant growth parameters observed are

plant height, stem diameter, number of leaves, leaf area, and metal content of Hg,

Zn, and Cu in plant organs. ANOVA with Duncan Multiple Range Test (DMRT)

were used for the analysis. The results showed that the treatment with manure has

an impact on the parameter of plant growth and bioaccumulation of Hg, Cu and

Zn in the plant organs. DMRT showed that the treatment with manures has a

significant influence on the growth and bioaccumulation of Hg, Cu, and Zn in the

plants. The manure with cows was better in supporting growth of silk tree

compared to those with chicken, goat as well as control. Treatment with manure

reduced bioaccumulation of Hg but increased bioaccumulation of Cu and Zn in

the plant organs. The bioaccumulation of Hg, Cu and Zn was found the highest in

the root than in the stem and leaves. The total bioaccumulation of Zn in plant

organs was the highest compared with that of Cu and Hg.

Keyword: Manure, Growth, Heavy Metals, Silk Tree, Ex-Gold Mining Land

1. Inroduction

Mining industry always received a great attention as it has high risk on

environment. It is often found that mining practices without good planning have

caused great environmental damage [38]. Improper handling of mining land has

caused the government to spend much more to restore the ecological, social and

economical function of the environment than the benefits received [1, 5, 7, 10].

The ex-mining land is often left unattended and unplanted in which this

have caused the land degraded, unproductive, and becoming marginal. If not

managed properly, it will decrease, for example, air quality due to dust, water

quality (physic and chemical qualities) due to erosion and sedimentation,

groundwater quantity and quality due to chemical pollution, the shift of land use

(change of topography, drainage, and vegetation), and the changing shape of the

land surface due to overburden piles. As a result of gold mining, chemical,

physical and biological damage can occur [8]. For example, the pollution of soil,

water and vegetation occurs due to the use of Hg (mercury) in leaching. The high

concentration of Cu and Zn was also detected on gold mining land in Bombana.

Such chemical content can be hazardous to the plant [8, 13]. The decrease of Cu

levels in soil solution has increased pH in soil as attached to the soil matrix. The

level of Zn in soil is higher at low pH than at high pH whereas the solubility of Zn

is higher in high acidity than in low acidity [2].

The deficiency of essential nutrients such as nitrogen and phosphorus, the

soil acidity (low pH) and mineral toxicity which are mainly due to heavy metals

such as mercury (Hg), copper (Cu) and zinc (Zn), are common and as the major

obstacles encountered in the ex-mining land [9], such as in the ex-gold mining

land in Bombana.

The extreme conditions of mining land can be handled in two ways: first,

the improvement of soil conditions with ameliorant engineering applications, for

Effect of manure and the bioaccumulation of heavy metals Hg, Cu and Zn 79

example, the user of organic and unorganic fertilizer to support the plant growth;

the second alternative is to choose plants that can adapt to such extreme

conditions [3].

In this research, the use of organic manure on ex-mining land, being

present abundant in Bombana, is studied. After being processed into organic

fertilizer, the organic manure was applied to the poor-nutrient ex-mining land.

The manure will support the availability of nutrients and improve the physical,

chemical and biological soil properties [9]. Sengon (Paraserianthes falcataria (L.)

Nielsen) was used as agents of phytoremediation to restore the ex-mining land

with heavy metal contamination as the plants can grow in poor, dry, muddy or

slightly salty soil [4].

2. Method

Material

The materials used in this study consist of; (i) sample of ex-mining soil, to

be analyzed its physicochemical properties and used it as a growing medium for

plant bioaccumulator screening; (ii) silk trees (Paraserianthes falcataria (L.)

Nielsen); (iii) polybags with size of 12 x 8 cm as container screening; (iv) water,

for watering plants during screening; (v) Chemical compounds, used for the

analysis of physicochemical properties of heavy metal levels, i.e., Hg, Cu and Zn,

in the ex-gold mining soil and in the plant organs.

Tools

A number of tools were used in this study such as; shovels, hoes, soil sieve

and the sack for taking ex-gold mining soil samples; stationery and camera for the

documentation; scales for weighting the ex-gold mining soil samples and plant

organs; multi tester (pH meter, Higro meters), Lux meter; GPS used for

determining the coordinates of a former quarry soil sampling; oven, filter paper,

glass-beaker, flask peck, Microwave oven, AAS, Computer as a data processor.

Procedure

This is an experimental research with a completely randomized design

(CRD). There are three units of animal manure treatment; i.e., crib, goat, chicken

manure, and one control unit or without manure, with five repetitions for each

unit, in total there are 20 units in the greenhouse experiments.

The procedure consisted of several steps; (i) conducting survey on ex-gold

mining sites in Bombana Regency; (ii) carring out analysis of soil sampling in

terms of physical and chemical properties of the soil character and as a growing

medium; (iii) preparing the growing plant media with the treatment of manure

(crib, goat, chicken) with the same dose of 150g/10kg soil, equivalent to 30

tonnes/ha. In addition to animal manure, the treatment for all growing media was


to put the same basic fertilizer; i.e., urea (1,5g/kg soil is equivalent to 300kg/ha),

SP-36 (1g/10kg of soil equivalent to 200kg/ha) and KCL (0,5 g/kg soil is

equivalent to 100kg/ha) as well as the addition of lime CaCO3 as much as

10g/10kg of soil equal to 2 ton ha-1 (Harry, 1994). Furthermore, bioaccumulator

screening of silk tree (Paraserianthes falcataria (L.) was grown in the green

house; plant maintenance such as watering is done daily and measure growth

parameters every two weeks; analyze plant growth (height, stem diameter, number

of leaf including leaf area) and bioaccumulation of Hg, Cu, Zn in plant organs.

The data relating to the growth and the concentration of heavy metals (Hg,

Cu, Zn) was obtained from the measurements using AAS tool for the entire

sample in the test ANOVA (analysis of variance) in SPSS software. The

corelation between the heavy metal concentrations in the parts of the plant and

those in the soil was analyzed with Duncan Multiple Range Test (DMRT). The

correlation between two factors is statistically significant if p-value is less than

0.05 (p<0.05).

3. Result and Discussion

The results showed that the treatment with cow manure, goat manure and

chicken manure significantly affect on the growth and the bioaccumulation of

heavy metals Hg, Cu, and Zn in the plant organs silk tree (Paraserianthes

falcataria (L.) Nielsen) grown on ex-gold mining land. For more specific, the

results of each parameter observed are described as follows:

a. Plant Height

The average plant height on the silk tree (Paraserianthes falcataria (L.)

Nielsen) without manure treatment (control) and with manure (crib, goat, chicken)

can be seen in Table 1.

Tablel 1. Plant Height of Silk Tree (Paraserianthes falcataria (L.) Nielsen) (cm)

P Plant Height (cm) in 0 - 12 Weeks

Means 0 2 4 6 8 10 12

C 13,34 14,28 16,38 19,84 20,42 22,17 24,56 18,57a

S 15,99 23,84 29,24 34,44 41,64 47,08 50,82 35,29b

K 15,14 17,56 20,18 27,06 28,44 30,2 33,5 22,58ab

A 14,46 17,84 24,01 29,32 33,04 38,17 40,02 28,12ab

Two means followed by the same letters in the same column indicate they are

not significantly different (p=0.05). P = Animal manure Treatments: C =

Control, S = Cow, K = Goat and A = Chicken.

The addition of organic matter (manure) into the soil has resulted in a

positive response to the plant growth. This study showed that the treatment with manure as organic material supplied to the plant growing medium resulted in better

10

20

30

40

50

60

0 2 4 6 8 10 12

C= Control

S= Crib

K= Goat

A= Henhouse

CSKA

Hig

h p

lant (c

m)

Time (Weeks)


growth on the silk tree (Paraserianthes falcataria (L.) Nielsen) than those planted

on the medium without treatment of animal manure.

The results also showed that the treatment with different manure gave the

different effect on the plant growth of silk tree (Paraserianthes falcataria (L.)

Nielsen) even though the same dose of each manure was applied to the treatment

units, that was 150g/10kg. The study showed that the average plant height silk

tree (Paraserianthes falcataria (L.) Nielsen) planted in the ex-gold mining soil

media was as follows; in the media with the treatment of cow manure (35.29 cm),

henhouse manure (28.12 cm), goat manure (22.58 cm) and controls (18.57 cm).

The average height of silk tree planted in the media with the treatment of cow

manure was significantly different from the height in the controls but it was not

significantly different with the height in chicken manure and manure goat.

The significant difference on the silk tree growth between the treatment

with and without manure is an evidence that manure is very helpful in providing

essential macro and micro nutrients useful to support the plant growth.

The composition of nutrition contained in cow manure is best suited to

support the hieght of sengon plants. The content of NPK element in the cow

manure on the land, applied to ex-gold mining soil, is used as a medium to grow

plants sengon (Paraserianthes falcataria (L.) Nielsen) which consists of N 0.58%,

12.67% P, K 0.53%; Goat manure N 0.41%, 11.24% P, K 0.31%; and chicken

manure, i. e., 0.37% of N, P and K 11.35% 0.36% [35]. From the composition of

macro nutrients NPK, it can be seen that the content of the cow manure is higher

than the other fertilizers in which the plant growth of silk tree (Paraserianthes

falcataria (L.) Nielsen) with cow manure is better than the plant growth on goat

and chicken manures. This is clearly shown in plant height charts and graphs in

which there is a relatively high growth rate on sengon plants planted in the ground

ex-gold mining land with cow manure until the age of 12 weeks after planting, as

depicted in Figures 1 and 2.

Figure1. Graph of Plant Height

(cm) 0-12 weeks

Figure 2. Relative growth rate of plant

height (cm) 0-12 weeks

8 10

Time (weeks)

1

2

3

4

5

6

2 MST 4 MST 6 MST 8 MST 10 MST 12 MST

CSKA

1,4

1,5

1,6

1,7

1,8

1,9

2

2 4 6

= Control = Crib = Goat = Henhouse

12


Based on the analysis of plant height increment for difference manure as in

Table 1, it indicates that the treatment of cow (crib) manure. The biggest

difference on the plant height increment with cow treatment occurs at week 8, that

is around 7.2 cm, with goat manure treatment at week 6 with 6,66 cm and with

chicken (hen house) manure treatment at week 4 with 5.31 cm. The high

increment on the plant growth with goat and chicken manure occurs in the early

growth of plants which is due to the fact that the goat and henhouse manure is a

fertilizer with quick microorganism heat and therefore its availability in the

planting medium becomes quickly exhausted. While the highest plant height

increment in the treatment of cow manure occurs at the end of plant growth, due

to the fact that cow manure is a cold fertilizer and the supply of available nutrients

to the plants takes longer. Thus, the dvantages of cold manure nutrients are that

they are present in the cow manure for longer period of time in the plant growth

media.

b. Stem Diameters

The observation of the average stem diameters of the silk tree

(Paraserianthes falcataria (L.) Nielsen) without (control) and with manure

treatment (crib, goat and henhouse) can be seen in Table 2.

Table 2. Stem Diameter of Silk Tree (Paraserianthes falcataria (L.) Nielsen)

(cm)

P Stem Diameter (cm) in 0 - 12 Weeks

Means 0 2 4 6 8 10 12

C 0,84 0,96 1,06 1,2 1,32 1,46 1,49 1,19a

S 1,58 1,78 2,06 2,58 2,99 3,55 3,95 2,64b

K 1 1,18 1,68 1,99 2,29 2,39 2,49 1,86a

A 1,28 1,48 2,01 2,68 2,89 2,98 3,12 2,35b

Means followed by the same letters, in same column was not significantly

different (p=0.05). P= Animal manure; C=Control, S= Cow, K= Goat, A=

Chicken.

The treatment of manure is also a significant effect on the increase in stem

diameter of plants silk tree (Paraserianthes falcataria (L.) Nielsen). DMRT

results showed that the increase of stem diameter in the silk tree plants with the

treatment of cow manure is significantly different from those with the goat

manure treatment and control but it is not different from those with henhouse

manure treatment. The results showed that the largest growth in diameter 2.6 cm

for the cow manure, 2.35 cm for the henhouse manure, 1.86 cm for goat manure

and the lowest is 1.19 cm for controls. The lower in the magnitude of the diameter

for the treatment with cow manure is presumably because the element of K

(potassium) in the cow manure is greater than K elements being present in goat

and henhouse manure. This element K is used for secondary cell division by meri-

0.5

1

1.5

2

2.5

3

3.5

4

0 2 4 6 8 10 12

C= Control

S= Crib

K= Goat

A= Henhouse

CSKA

Ste

m D

iam

ete

rs (

cm

)

Time (Weeks)


stematic activities of stem cells which tend to widen and effect on stem diameter

and biomass.

Relative growth rate of the largest diameter silk tree plant with cow

manure treatment is 0,507cm/2 weeks and lowest is in the control, that is

0,168cm/2 weeks. Based on the analysis of variance (ANOVA), it showed that the

manure treatment significantly influence the control where the p-value is less than

0.05. This indicates that the use of manure can increase the growth rate relative

diameter stem of the plant. The silk tree stem diameter and its relative growth rate

can be seen in Figures 3 and Figure 4.

Figure 3. Graph of stem diameter

of silk tree (Paraserianthes

falcataria (L.) Nielsen) (cm)

Figure 4. Relative growth rate of stem

diameter of silk tree (Paraserianthes

flacataria (L.) Nielsen) (cm)

c. Leaf Area and Number of Plant Leaves

The observation of the average number of silk tree (Paraserianthes

falcataria (L.) Nielsen) plant leaves without (control) and with manure (cow, goat

and chicken) can be seen in Table 3.

Table 3. Number of Plant Leaves on Silk Tree (Paraserianthes falcataria (L.)

Nielsen)

P Number of Plant Leaves (Pieces)

Means 0 2 4 6 8 10 12

C 2,4 2,6 3,1 3,5 4,4 4,8 5,2 3,71a

S 3 3,8 5 6,9 8,2 9,22 10,27 6,63b

K 2,1 2,6 4,6 4,91 5,03 5,09 6,03 4,04ab

A 2,2 2,91 5,09 6,01 6,99 7,06 7,89 5,45b


different (p=0.05). P= Animal manure; C=Control, S= Cow, K= Goat, A=

Chicken.

0

0,1

0,2

0,3

0,4

0,5

0,6

0,7

2 4 6 8 10 12

1

2

3

4

5

6

2 MST 4 MST 6 MST 8 MST 10 MST 12 MST

CSKA

Time (weeks)

= Control = Crib = Goat = Henhouse

5

10

15

20

25

30

35

0 2 4 6 8 10 12

C= Control

S= Crib

K= Goat

A= Henhouse

CSKA

Leaf

Are

a (

cm2)

Time (Weeks)


Based on Table 3 shown the average number of leaves (pieces) silk tree

(Paraserianthes falcataria (L.) Nielsen) more on the treatment of cow manure

(6,33 strands), henhouse manure (5.45 strands), goat manure (strands 4.04) and

the lowest number of leaves on the control (3.71 strands). Based on analysis of

variance (ANOVA) showed that manure application has a significant effect on the

number of plant leaves sengon (p-value <0.05) and a further test results DMRT

showed that the average number of leaves with cow manure is significantly

different from that for the control but not significantly different from that with

henhouse manure. Based on ANOVA statistical test and DMRT results, they

showed that the leaf area (cm2) also showed a similar result to the number of

leaves on silk tree, as shown in Table 4 and Figure 5.

Table 4. Leaf Area (Cm2) of Silk Tree (Paraserianthes falcataria (L.) Nielsen)

P Leaf Area (cm2)

Means 0 2 4 6 8 10 12

C 6,57 7,38 8,28 8,62 9,03 10,22 13,21 9,04a

S 9,78 10,37 10,74 16,11 21,68 27,23 32,25 18,31b

K 9,15 9,37 14,63 15,22 17,73 18,83 20,26 13,03ab

A 9,62 10,05 16,28 18,83 20,2 22,49 23,88 17,34b


different (p=0.05). P= Animal manureTreatments: C= Control, S= Cow, K=

Goat, A= Chicken.

Figure 5. Graph of leaf area (cm2)

d. Percentage and bioaccumulation of Heavy Metal in Plant Organs

The percentage of metal bioaccumulation of Hg, Cu, and Zn presented in

the plant organs; roots, stems and leaves of plants, both on the control (without

manure) and on the manure treatment (cow, goat, and chicken) can be seen in

Figure 6-8.


Figure 6. Diagram of Hg bioaccumulation on plant organs that translocate to leaf,

stems and roots after 12 weeks planting. , ,

Figure 7. Diagram of Cu bioaccumulation on plant organs that translocate to leaf,

stems and roots after 12 weeks planting. , ,

Figure 8. Diagram of Zn bioaccumulation on plant organs that translocate to leaf,

stems and roots after 12 weeks planting , ,

Total bioaccumulation of Hg, Cu and Zn in plant organs of silk tree on the

control (without manure) and with manure treatment (crib, goat and henhouse)

can be seen in Table 5-7.

Table 5. Bioaccumulation of Hg in plant organs silk tree (ppm)

P Soil Bioaccumulation of Hg (ppm) Total in

Plant

Organs Before After

Roots Stems Leaves

C

6,5

0,0201a 0,0094a 0,0043a 0,0007a 0,0144

S 0,0460b 0,0061b 0,0019b 0,0006a 0,0086

K 0,0463b 0,0047b 0,0007b 0,0004a 0,0058

A 0,0399b 0,0081b 0,0033b 0,0005a 0,0119


different (p=0.05). P= Animal manure; C= Control, S= Cow, K= Goat, A=

Chicken.

C S K A

C K A

C K A S


Table 6. Bioaccumulation of Cu in plant organs silk tree (ppm)

P Soil Bioaccumulation of Cu (ppm) Total in Plant

organs Before After Roots Stems Leaves

C

644,79

0,3051a 0,1449a 0,1255a 0,0858a 0,3562

S 0,4133a 0,2082a 0,1908a 0,1133b 0,5123

K 0,4592a 0,1837b 0,1745b 0,1041b 0,4623

A 0,2118a 0,3010b 0,1990b 0,1286b 0,6286


different (p=0.05). P = Animal manure; C= Control, S= Cow, K= Goat, A=

Chicken.

Table 7. Bioaccumulation of Zn in plant organs silk tree (ppm)

P Soil Bioaccumulation of Cu (ppm) Total in

Plant organs Before After Roots Stems Leaves

C

360

1,6080a 0,8148a 0,5986a 0,5986a 2,012

S 1,7852a 0,8161a 0,8184a 0,6850b 2,320

K 1,7573a 0,8715a 0,8282b 0,7393b 2,439

A 1,6693a 0,8237a 0,6889a 0,6293b 2,142


different (p=0.05). P= Animal manure; C= Control, S= Cow, K= Goat, A=

Chicken.

The results from metal content analysis indicate that the bioaccumulation

of Hg, Cu and Zn were present in the supreme organ of the plant from the roots to

stems and leaves. The difference is due to bioaccumulation. According to [6], the

absorption and accumulation of heavy metals in plants can be divided into three

continuous process, i.e., metal uptaking by the root, metal translocating from the

roots to other plant parts and metal localizing on specific organs to maintain order

but not to inhibit the metabolism of the plant.

Bioaccumulation of Hg, Cu and Zn in the root organ due to the soil media

has a high metal content and the roots are muselec organ that can bind heavy

metals being present in the root. This is the reason that the metal is present more

in the roots than other plant organs. After the metal is transported into the root

organ, it is then transported, via the transport tissue, namely, xylem and phloem,

to the other plant organs. To improve the efficiency of transport, metal is bound

by the chelate molecules. According to [14], the absorption amount of heavy

metals in plant roots can also be due to the process lignification of the root and the

cessation of metal transport toward the leaves so that the metal accumulates in the

roots.

Based on the results of heavy metals (Hg, Cu and Zn) in silk tree

(Paraserianthes falcataria (L.) Nielsen) grown on ex-gold mining land, it showed

that metal accumulation in plant organs at the age of 3 months is, from the highest to the lowest concentration, Zn, Cu and Hg, respectively. This is because the percen-


tage of Zn nutrients needed by plants to grow is higher than the percentage of

metal elements, Cu and Hg, respectively, despite the presence of Hg is more on

the ground [14].

The ccumulation of heavy metal Zn in the silk tree organs is higher than

that of Cu and Hg. This is because the metal Zn is an essential element for the

growth of all kinds of animals and plants. Zn is found virtually in all cells and it is

a very important element for the growth of human, animal or plant after Fe. Zn

role in catalytic reaction, i.e., almost 100 types of enzymes with the ability

catalyst in the reaction, depends on Zn. Zinc also plays an important role in

developing and stabilizing the protein structure of the cell membrane structure and

it is also as a catalyst enzyme superoxide (CuZnSOD) [11].

5. Conclusion

It was shown that animal manure has a significant influence on the growth

of silk trees planted in the ex-gold mining land of Bombana Southeast Sulawesi.

Moreover, it was found that the cow manure has the best effect in increasing the

plant height, stem diameters, leaf area, the number of leaves and the root length.

The highest bioaccumulation percentage of heavy metal; Hg, Cu and Zn,

was found in roots compared those found on stems and leaves of silk tree organs

(Paraserianthes falcataria (L.) Nielsen). Total bioaccumulation of Hg in the plant

organs was higher on the control group than on the manures treatment. The

highest bioaccumulation of Cu was found on the tree with chicken manure,

whereas the highest bioaccumulation of Zn was in the trees with goat manure. The

higher accumulation of heavy metals found in the silk tree organs was Zn

compared to the accumulation of Cu and Hg.

Acknowledgements. First author would like to thanks the Ministry of Higher

Education of Indonesian government for the research funding through Hibah

Bersaing scheme. We express our thanks to PT. Panca Logam Makmur (mining

industrial company), located in District of Bombana, the Province of Southeast

Sulawesi, for their permission to collect soil sample from ex gold mining land.

We also extend our thanks to the head of the department of Biology, Universitas

Halu Oleo, for allowing us to conduct our research in the experimental Glass

House of Biology Laboratory, Department of Biology, FMIPA, UHO.

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Received: April 27, 2016; Published: July 3, 2016

http://dx.doi.org/10.5402/2011/402647

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